Is chemosensory input essential for the rapid rejection of toxic foods?

Abstract

Herbivorous insects often rapidly reject foods containing toxic plant compounds. While the functional significance of this rejection response is clear, the mechanistic basis is not. The role of peripheral chemoreceptors in the rapid rejection of toxic foods was examined using a model system consisting of nicotine and the tobacco hornworm (Manduca sexta), which is a pest of tobacco plants. When offered diets containing naturally occurring concentrations of nicotine, larvae initially fed readily, but abruptly stopped feeding within 30s. A high percentage of larvae also exhibited toxic responses mediated by the central nervous system (twitching and writhing) to the ingested nicotine within 30s, indicating that nicotine could have been absorbed within the same time as the rejection response. Two lines of evidence are provided against a role of peripheral chemoreceptors in this rapid rejection response. First, all mouthpart chemoreceptors were ablated from the larvae, and they were then subjected to feeding tests with diets containing either nicotine or a compound (caffeine) that is known to stimulate deterrent taste receptors in M. sexta. Whereas the ablations virtually eliminated the rejection response to caffeine, they had no measurable impact on the rejection response to nicotine. Second, sensory recordings from two important gustatory sensilla (the medial and lateral styloconica) failed to demonstrate a plausible role of sensory input from either sensillum in the rapid rejection of nicotine. The most parsimonious interpretation of these results is that the nicotine rejection response was mediated by a rapidly acting post-ingestive mechanism.